Skip to main content
Log in

Exposure to low levels of photosynthetically active radiation induces rapid increases in palisade cell chloroplast volume and thylakoid surface area in sunflower (Helianthus annuus L.)

  • Original Papers
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Sudden changes in photoactive radiation (PAR) (wavelength, 400–700 nm) induces rapid surface area changes in chloroplast thylakoid membranes. Although this response may have important photo-acclimative functions for the plant, little is known about the mechanisms by which changes in irradiance are detected or how thylakoid membranes actually increase or decrease surface area. Knowledge of the time required for significant changes in thylakoid area would help eliminate or support several possible mechanisms that may be involved in this aspect of photo-acclimation in plants. Leaf tissues were acclimated to a PAR of 500 μmol quanta per m2 per s then exposed to low irradiance (PAR, 50 μmol quanta per m2 per s) and sampled at 5, 15, 30, and 60 min post exposure. Tissue and cell structure were quantified and results showed a significant increase in the surface-to-volume ratio and surface area per unit of standard leaf volume for both appressed and nonappressed thylakoids within 5 min of exposure to low irradiance. On the basis of the ratios of appressed to nonappressed thylakoids, the surface area of the nonappressed thylakoids was found to increase faster than that of the appressed thylakoids throughout the sample period. The portion of the appressed thylakoids in contact with the stroma was defined as margin thylakoids. Margin thylakoid surface-to-volume ratio did not change relative to the high-irradiance control during the sample period but did remain significantly lower than the low-irradiance control during the sample period. The ratio of appressed to margin thylakoids indicated a broadening and shortening of the appressed thylakoid stack within the first 5 min of low-irradiance exposure. The rapidity of the shade response indicates that the early events in this response probably do not directly involve gene activation pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

PAR:

photosynthetically active radiation

Sv:

surface to volume density

Vv:

volume density

UV-B:

ultraviolet B radiation

References

  • Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37: 93–136

    Google Scholar 

  • —, Aro EM (1994) Grana stacking and protection of photosystem II in thylakoid membranes of higher plant leaves under sustained high irradiance: an hypothesis. Photosynth Res 41: 315–326

    Google Scholar 

  • —, Osmond CB (1987) Shade-sun responses: compromises between acclimation and photoinhibition. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 1–38

    Google Scholar 

  • —, Chow WS, Goodchild DJ (1988) Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15: 11–26

    Google Scholar 

  • — —, Park YI (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46: 129–139

    Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, New York, pp 227–289

    Google Scholar 

  • Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28: 355–377

    Google Scholar 

  • Dawes CJ (1988) Introduction to biological electron microscopy: theory and techniques. Ladd Research Industries. Burlington, Vt

    Google Scholar 

  • Epstein MA, Holt SJ (1963) The localization by electron microscopy of HeLa cell surface enzymes splitting adenosine triphosphate. J Cell Biol 19: 325–326

    Google Scholar 

  • Fagerberg WR (1980) Stereology: quantitative electron microscopic analysis. In: Gantt E (ed) Handbook of phycological methods: developmental and cytological methods. Cambridge University Press, New York, pp 392–400

    Google Scholar 

  • —, (1983) A quantitative study of daily variation in the cellular ultrastructure of palisade chlorenchyma from sunflower leaves. Ann Bot 52: 117–126

    Google Scholar 

  • —, (1987) Effect of short-term shading on the cytology of palisade tissue in mature leaves of the sunflowerHelianthus annuus. Am J Bot 74: 822–828

    Google Scholar 

  • —, (1988a) Stereology. In: Dawes CJ, Introduction to biological electron microscopy: theory and techniques. Ladd Research Industries, Burlington, Vt, pp 265–281

    Google Scholar 

  • —, (1988b) The effect of neutral shade on the structure of mature sun-acclimated palisade cells ofHelianthus annuus. L. II: 3-day exposure. Bot Gaz 149: 295–302

    Google Scholar 

  • —, (1990) Changes in thylakoid surface area when shade acclimatedHelianthus annuus L. chloroplasts are exposed to high P. F. D. In: Baltscheffsky M (ed) Current research in photosynthesis, vol IV. Kluwer, Dordrecht, pp 385–388

    Google Scholar 

  • —, Bornman JF (1997) Ultraviolet-B radiation causes shade-type ultrastructural changes inBrassica napus. Physiol Plant 101: 833–844

    Google Scholar 

  • —, Culpepper G (1984) A morphometric study of anatomical changes during leaf development under low light conditions in sunflower. Bot Gaz 145: 346–350

    Google Scholar 

  • Ghoshroy S, Fagerberg WR (1998) Light detection system in mature sunflower chloroplasts; pigment mediated or total photon flux density related. Int J Plant Sci 159: 110–115

    Google Scholar 

  • Hoober JK, White RA, Marks DB, Gabriel JL (1994) Biogenesis of thylakoid membranes with emphasis on the process inChlamydomonas. Photosynth Res 39: 15–31

    Google Scholar 

  • Huner NPA, Maxwell D, Gray DP, Savitch V, Krol M, Ivanov AG, Falk S (1996) Sensing environmental temperature change through imbalances between energy supply and energy consumption: redox state of photosystem II. Physiol Plant 98: 358–364

    Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol 77: 483–485

    Google Scholar 

  • Joyard J, Block MA, Dorne AJ, Coves J, Pineaur B, Douce R (1986) The chloroplast envelope membrane: a key structure in chloroplast biogenesis. In: Akryunoglou G, Senger H (eds) Regulation of chloroplast differentiation. Alan R Liss, New York, pp 217–228

    Google Scholar 

  • —, Teyssier E, Miège C, Gerny-Seigneurin D, Marèchal E, Block MA, Dorne A-J, Rolland N, Ajlani G, Douce R (1998) The biochemical machinery of plastid envelope membranes. Plant Physiol 118: 715–723

    Google Scholar 

  • Lichtenthaler HK, Buschmann C, Rahmdorf U (1980) The importance of blue light for the development of sun-type chloroplasts. In: Senger H (ed) The blue light syndrome. Springer, Berlin Heidelberg New York, pp 485–494

    Google Scholar 

  • Mäenpää P, Aro E-M (1986) Chlorophyll-protein complexes, chlorophyll a/b ratio and chloroplast ultrastructure inLemna minor M. grown under different light conditions. J Plant Physiol 123: 161–168

    Google Scholar 

  • Malkin S, Canaani O, Havaux M (1986) Analysis of Emerson enhancement under conditions where photosystem II is inhibited: are the two photosystems indeed separated? Photo Res 10: 291–296

    Google Scholar 

  • Park Y-LL, Chow W, Anderson JM (1995a) The quantum yield of photoinactivation of photosystem II in pea leaves is greater at low than high photon exposure. Plant Cell Physiol 36: 1163–1167

    Google Scholar 

  • — — — (1995b) Light inactivation of functional photosystem II in leaves of peas grown in moderate light depends on photon exposure. Planta 196: 401–411

    Google Scholar 

  • Peracchia C, Mittler BS (1972) Fixation by means of glutaraldehydehydrogen peroxide reaction products. J Cell Biol 53: 234–238

    Google Scholar 

  • Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397: 625–628

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208–212

    Google Scholar 

  • Trissl H-W, Wilhelm C (1993) Why do thylakoids membranes from higher plants form grana stacks. Trends Biochem Sci 18: 415–419

    Google Scholar 

  • Voskresenskaya NP (1984) Control of the activity of photosynthetic apparatus in higher plants. In: Senger H (ed) Blue light effects in biological systems. Springer, Berlin Heidelberg New York Tokyo, pp 407–418

    Google Scholar 

  • Weibel ER (1979) Stereological methods, vol I, practical methods for biological morphometry. Academic Press, New York

    Google Scholar 

  • —, Bolender RR (1973) Stereological techniques for electron microscopic morphometry. In: Hayat MA (ed) Principles and techniques of electron microscopy: biological applications, vol III. Van Nostrand Reinhold, New York, pp 237–296

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wheeler, W.S., Fagerberg, W.R. Exposure to low levels of photosynthetically active radiation induces rapid increases in palisade cell chloroplast volume and thylakoid surface area in sunflower (Helianthus annuus L.). Protoplasma 212, 38–45 (2000). https://doi.org/10.1007/BF01279345

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01279345

Keywords

Navigation